Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules

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Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules

JE Schnitzer, P Oh, E Pinney and J Allard
Department of Pathology, Harvard Medical School, Beth Israel Hospital, Boston, Massachusetts 02215.

Caveolae or noncoated plasmalemmal vesicles found in a variety of cells have been implicated in a number of important cellular functions including endocytosis, transcytosis, and potocytosis. Their function in transport across endothelium has been especially controversial, at least in part because there has not been any way to selectively inhibit this putative pathway. We now show that the ability of sterol binding agents such as filipin to disassemble endothelial noncoated but not coated plasmalemmal vesicles selectively inhibits caveolae-mediated intracellular and transcellular transport of select macromolecules in endothelium. Filipin significantly reduces the transcellular transport of insulin and albumin across cultured endothelial cell monolayers. Rat lung microvascular permeability to albumin in situ is significantly decreased after filipin perfusion. Conversely, paracellular transport of the small solute inulin is not inhibited in vitro or in situ. In addition, we show that caveolae mediate the scavenger endocytosis of conformationally modified albumins for delivery to endosomes and lysosomes for degradation. This intracellular transport is inhibited by filipin both in vitro and in situ. Other sterol binding agents including nystatin and digitonin also inhibit this degradative process. Conversely, the endocytosis and degradation of activated alpha 2- macroglobulin, a known ligand of the clathrin-dependent pathway, is not affected. Interestingly, filipin appears to inhibit insulin uptake by endothelium for transcytosis, a caveolae-mediated process, but not endocytosis for degradation, apparently mediated by the clathrin-coated pathway. Such selective inhibition of caveolae not only provides critical evidence for the role of caveolae in the intracellular and transcellular transport of select macromolecules in endothelium but also may be useful for distinguishing transport mediated by coated versus noncoated vesicles.
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Torgersen, M. L., Skretting, G., van Deurs, B., Sandvig, K. (2002). Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci. 114: 3737-3747 [Abstract] [Full Text]
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Mobius, W., Ohno-Iwashita, Y., van Donselaar, E. G., Oorschot, V. M.J., Shimada, Y., Fujimoto, T., Heijnen, H. F.G., Geuze, H. J., Slot, J. W. (2002). Immunoelectron Microscopic Localization of Cholesterol Using Biotinylated and Non-cytolytic Perfringolysin O. J. Histochem. Cytochem. 50: 43-56 [Abstract] [Full Text]
Vogel, S. M., Malik, A. B. (2002). Albumin transcytosis in mesothelium: further evidence of a transcellular pathway in polarized cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 282: L1-L2 [Full Text]
Ushio-Fukai, M., Hilenski, L., Santanam, N., Becker, P. L., Ma, Y., Griendling, K. K., Alexander, R. W. (2001). Cholesterol Depletion Inhibits Epidermal Growth Factor Receptor Transactivation by Angiotensin II in Vascular Smooth Muscle Cells. ROLE OF CHOLESTEROL-RICH MICRODOMAINS AND FOCAL ADHESIONS IN ANGIOTENSIN II SIGNALING. J. Biol. Chem. 276: 48269-48275 [Abstract] [Full Text]
Dzenko, K. A., Andjelkovic, A. V., Kuziel, W. A., Pachter, J. S. (2001). The Chemokine Receptor CCR2 Mediates the Binding and Internalization of Monocyte Chemoattractant Protein-1 along Brain Microvessels. J. Neurosci. 21: 9214-9223 [Abstract] [Full Text]
Vogel, S. M., Minshall, R. D., Pilipovic', M., Tiruppathi, C., Malik, A. B. (2001). Albumin uptake and transcytosis in endothelial cells in vivo induced by albumin-binding protein. Am. J. Physiol. Lung Cell. Mol. Physiol. 281: L1512-L1522 [Abstract] [Full Text]
Nowroozi, N., Kawata, T., Liu, P., Rice, D., Zernik, J. H. (2001). High {beta}-Galactosidase and Ganglioside GM1 Levels in the Human Parotid Gland. Arch Otolaryngol Head Neck Surg 127: 1381-1384 [Abstract] [Full Text]